Conserved rules govern genetic interaction degree across species
Open accessAbstract
Background: Synthetic genetic interactions have recently been mapped on a genome scale in the budding yeast Saccharomyces cerevisiae, providing a functional view of the central processes of eukaryotic life. Currently, comprehensive genetic interaction networks have not been determined for other species, and we therefore sought to model conserved aspects of genetic interaction networks in order to enable the transfer of knowledge between species. Results: Using a combination of physiological and evolutionary properties of genes, we built models that successfully predicted the genetic interaction degree of S. cerevisiae genes. Importantly, a model trained on S. cerevisiae gene features and degree also accurately predicted interaction degree in the fission yeast Schizosaccharomyces pombe, suggesting that many of the predictive relationships discovered in S. cerevisiae also hold in this evolutionarily distant yeast. In both species, high single mutant fitness defect, protein disorder, pleiotropy, protein-protein interaction network degree, and low expression variation were significantly predictive of genetic interaction degree. A comparison of the predicted genetic interaction degrees of S. pombe genes to the degrees of S. cerevisiae orthologs revealed functional rewiring of specific biological processes that distinguish these two species. Finally, predicted differences in genetic interaction degree were independently supported by differences in co-expression relationships of the two species. Conclusions: Our findings show that there are common relationships between gene properties and genetic interaction network topology in two evolutionarily distant species. This conservation allows use of the extensively mapped S. cerevisiae genetic interaction network as an orthology-independent reference to guide the study of more complex species.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The functional, physiological and evolutionary properties associated with genetic interaction frequency should predict genetic network connectivity and candidate genes that may serve as important genetic modifiers in other organisms, including humans.
“The functional, physiological and evolutionary properties associated with genetic interaction frequency should predict genetic network connectivity and candidate genes that may serve as important genetic modifiers in other organisms, including humans (25).”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [25]
The general topology of genetic networks will also be conserved.
“it is reasonable to expect that the general topology of genetic networks will also be conserved (25)”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [25]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
Full-length transcriptome assembly from RNA-Seq data without a reference genome
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., et al. (2011) · Nature Biotechnology · doi:10.1038/nbt.1883 · Cited by 20,770 · see citing works
Breiman, L. (1996) · Machine Learning · doi:10.1007/bf00058655 · Cited by 16,325 · see citing works
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,062 · see citing works
PAML 4: Phylogenetic Analysis by Maximum Likelihood
Yang, Z. (2007) · Molecular Biology and Evolution · doi:10.1093/molbev/msm088 · Cited by 13,879 · see citing works
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository
Edgar, R. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.207 · Cited by 13,288 · see citing works
EMBOSS: the European molecular biology open software suite.
Rice, P., Longden, I., & Bleasby, A. (2000) · Trends in Genetics · doi:10.1016/s0168-9525(00)02024-2 · Cited by 9,466 · see citing works
MUSCLE: a multiple sequence alignment method with reduced time and space complexity
Edgar, R. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-113 · Cited by 8,948 · see citing works
The International HapMap Project
†The International HapMap Consortium, Genotyping centres: Baylor College of Medicine and ParAllele BioScience, Gibbs, R. A., Belmont, J. W., Hardenbol, P., Willis, T. D., Yu, F., Chinese HapMap Consortium, Yang, H., Ch'ang, L.-Y., et al. (2003) · Nature · doi:10.1038/nature02168 · Cited by 6,057 · see citing works
Missing Value Estimation Methods for DNA Microarrays
Troyanskaya, O., Cantor, M., Sherlock, G., Brown, P., Hastie, T., Tibshirani, R., Botstein, D., & Altman, R. B. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.6.520 · Cited by 4,230 · see citing works
BioGRID: a general repository for interaction datasets
Stark, C. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj109 · Cited by 3,960 · see citing works
Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1
Barbie, D. A., Tamayo, P., Boehm, J. S., Kim, S. Y., Moody, S. E., Dunn, I. F., Schinzel, A. C., Sandy, P., Meylan, E., Scholl, C., et al. (2009) · Nature · doi:10.1038/nature08460 · Cited by 3,869 · see citing works
The Pfam protein families database
Punta, M., Coggill, P. C., Eberhardt, R. Y., Mistry, J., Tate, J., Boursnell, C., Pang, N., Forslund, K., Ceric, G., Clements, J., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gkr1065 · Cited by 3,719 · see citing works
The Genetic Landscape of a Cell
Costanzo, M., Baryshnikova, A., Bellay, J., Kim, Y., Spear, E. D., Sevier, C. S., Ding, H., Koh, J. L. Y., Toufighi, K., Mostafavi, S., et al. (2010) · Science · doi:10.1126/science.1180823 · Cited by 2,162 · see citing works
Self-citationEstimating Synonymous and Nonsynonymous Substitution Rates Under Realistic Evolutionary Models
Yang, Z., & Nielsen, R. (2000) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a026236 · Cited by 1,747 · see citing works
Dissecting the regulatory circuitry of a eukaryotic genome
Holstege, F. C. P., Jennings, E. G., Wyrick, J. J., Lee, T. I., Hengartner, C. J., Green, M. R., Golub, T. R., Lander, E. S., & Young, R. A. (1998) · Cell · doi:10.1016/s0092-8674(00)81641-4 · Cited by 1,670 · see citing works
NCBI GEO: archive for functional genomics data sets--10 years on
Barrett, T., Troup, D. B., Wilhite, S. E., Ledoux, P., Evangelista, C., Kim, I. F., Tomashevsky, M., Marshall, K. A., Phillippy, K., Sherman, P. M., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1184 · Cited by 1,127 · see citing works
A Genome-wide RNAi Screen Identifies Multiple Synthetic Lethal Interactions with the Ras Oncogene
Luo, J., Emanuele, M. J., Li, D., Creighton, C. J., Schlabach, M. R., Westbrook, T. F., Wong, K.-K., & Elledge, S. J. (2009) · Cell · doi:10.1016/j.cell.2009.05.006 · Cited by 1,017 · see citing works
Principles for the buffering of genetic variation
Hartman, J. L., Garvik, B., & Hartwell, L. (2001) · Science · doi:10.1126/science.1056072 · Cited by 808 · see citing works
Principles for the Buffering of Genetic Variation
Hartman IV, J. L. (2001) · Science · doi:10.1126/science.291.5506.1001 · Cited by 808 · see citing works
Analysis of a genome-wide set of gene deletions in the fission yeast Schizosaccharomyces pombe
Kim, D.-U., Hayles, J., Kim, D., Wood, V., Park, H.-O., Won, M., Yoo, H.-S., Duhig, T., Nam, M., Palmer, G., et al. (2010) · Nature Biotechnology · doi:10.1038/nbt.1628 · Cited by 742 · see citing works
PyEvolve: a toolkit for statistical modelling of molecular evolution
Butterfield, A., Vedagiri, V., Lang, E., Lawrence, C., Wakefield, M. J., Isaev, A., & Huttley, G. A. (2004) · BMC Bioinformatics · doi:10.1186/1471-2105-5-1 · Cited by 726 · see citing works
Genome-Wide RNAi Analysis of Growth and Viability in Drosophila Cells
Boutros, M., Kiger, A. A., Armknecht, S., Kerr, K., Hild, M., Koch, B., Haas, S. A., Paro, R., & Perrimon, N. (2004) · Science · doi:10.1126/science.1091266 · Cited by 702 · see citing works
The DISOPRED server for the prediction of protein disorder
Ward, J. J., McGuffin, L. J., Bryson, K., Buxton, B. F., & Jones, D. T. (2004) · Bioinformatics · doi:10.1093/bioinformatics/bth195 · Cited by 684 · see citing works
Issel‐Tarver, L., Christie, K., Dolinski, K. J., Andrada, R., Balakrishnan, R., Ball, C. A., Binkley, G., Dong, S., Dwight, S. S., Fisk, D. G., et al. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)50972-1 · Cited by 672 · see citing works
InParanoid 7: new algorithms and tools for eukaryotic orthology analysis
Ostlund, G., Schmitt, T., Forslund, K., Kostler, T., Messina, D. N., Roopra, S., Frings, O., & Sonnhammer, E. L. L. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp931 · Cited by 623 · see citing works
Natural history and evolutionary principles of gene duplication in fungi
Wapinski, I., Pfeffer, A., Friedman, N., & Regev, A. (2007) · Nature · doi:10.1038/nature06107 · Cited by 614 · see citing works
Schroer, T. A. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.012103.094623 · Cited by 614 · see citing works
Scholl, C., Fröhling, S., Dunn, I. F., Schinzel, A. C., Barbie, D. A., Kim, S. Y., Silver, S. J., Tamayo, P., Wadlow, R. C., Ramaswamy, S., et al. (2009) · Cell · doi:10.1016/j.cell.2009.03.017 · Cited by 539 · see citing works
Lehner, B., Crombie, C., Tischler, J., Fortunato, A., & Fraser, A. G. (2006) · Nature Genetics · doi:10.1038/ng1844 · Cited by 502 · see citing works
Comparative functional genomics of the fission yeasts
Rhind, N., Chen, Z., Yassour, M., Thompson, D. A., Haas, B. J., Habib, N., Wapinski, I., Roy, S., Lin, M. F., Heiman, D. I., et al. (2011) · Science · doi:10.1126/science.1203357 · Cited by 484 · see citing works
Genotype to Phenotype: A Complex Problem
Dowell, R. D., Ryan, O. W., Jansen, A., Cheung, D., Agarwala, S. D., Danford, T., Bernstein, D. A., Rolfe, A., Heisler, L. E., Chin, B., et al. (2010) · Science · doi:10.1126/science.1189015 · Cited by 415 · see citing works
Self-citationQuantitative analysis of fitness and genetic interactions in yeast on a genome scale
Baryshnikova, A., Costanzo, M., Kim, Y., Ding, H., Koh, J., Toufighi, K., Youn, J.-Y., Ou, J., San Luis, B.-J., Bandyopadhyay, S., et al. (2010) · Nature Methods · doi:10.1038/nmeth.1534 · Cited by 364 · see citing works
Self-citationConservation and Rewiring of Functional Modules Revealed by an Epistasis Map in Fission Yeast
Roguev, A., Bandyopadhyay, S., Zofall, M., Zhang, K., Fischer, T., Collins, S. R., Qu, H., Shales, M., Park, H.-O., Hayles, J., et al. (2008) · Science · doi:10.1126/science.1162609 · Cited by 352 · see citing works
Replication Checkpoint Enforced by Kinases Cds1 and Chk1
Boddy, M. N., Furnari, B., Mondesert, O., & Russell, P. (1998) · Science · doi:10.1126/science.280.5365.909 · Cited by 316 · see citing works
Genome-Wide RNAi Screen for Host Factors Required for Intracellular Bacterial Infection
Agaisse, H., Burrack, L. S., Philips, J. A., Rubin, E. J., Perrimon, N., & Higgins, D. E. (2005) · Science · doi:10.1126/science.1116008 · Cited by 308 · see citing works
Systematic Mapping of Genetic Interaction Networks
Dixon, S. J., Costanzo, M., Baryshnikova, A., Andrews, B., & Boone, C. M. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.114751 · Cited by 290 · see citing works
Self-citationeSGA: E. coli synthetic genetic array analysis
Butland, G., Babu, M., Díaz-Mejía, J. J., Bohdana, F., Phanse, S., Gold, B., Yang, W., Li, J., Gagarinova, A. G., Pogoutse, O., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1239 · Cited by 256 · see citing works
Self-citationWhere does fission yeast sit on the tree of life?
Sipiczki, M. (2000) · Genome biology · doi:10.1186/gb-2000-1-2-reviews1011 · Cited by 243 · see citing works
High-throughput, quantitative analyses of genetic interactions in E. coli
Typas, A., Nichols, R. J., Siegele, D. A., Shales, M., Collins, S. R., Lim, B., Braberg, H., Yamamoto, N., Takeuchi, R., Wanner, B. L., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1240 · Cited by 236 · see citing works
GeneDB: a resource for prokaryotic and eukaryotic organisms
Hertz‐Fowler, C. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh007 · Cited by 235 · see citing works
InParanoid 6: eukaryotic ortholog clusters with inparalogs
Berglund, A., Sjölund, E., Östlund, G., & Sonnhammer, E. L. L. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm1020 · Cited by 218 · see citing works
Discovery of biological networks from diverse functional genomic data
Myers, C. L., Robson, D. N., Wible, A., Hibbs, M., Chiriac, C., Theesfeld, C. L., Dolinski, K. J., & Troyanskaya, O. G. (2005) · Genome biology · doi:10.1186/gb-2005-6-13-r114 · Cited by 213 · see citing works
Self-citationDixon, S. J., Fedyshyn, Y., Koh, J. L. Y., Prasad, T. S. K., Chahwan, C., Chua, G., Toufighi, K., Baryshnikova, A., Hayles, J., Hoe, K.-L., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806261105 · Cited by 205 · see citing works
Self-citationSynthetic Genetic Array (SGA) Analysis in Saccharomyces cerevisiae and Schizosaccharomyces pombe
Baryshnikova, A., Costanzo, M., Dixon, S. J., Vizeacoumar, F. J., Myers, C. L., Andrews, B., & Boone, C. M. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(10)70007-0 · Cited by 201 · see citing works
Self-citationA global analysis of genetic interactions in Caenorhabditis elegans
Byrne, A. B., Weirauch, M. T., Wong, V., Koeva, M., Dixon, S. J., Stuart, J. M., & Roy, P. J. (2007) · Journal of Biology · doi:10.1186/jbiol58 · Cited by 172 · see citing works
Yoshida, T., Toda, T., & Yanagida, M. (1994) · Journal of Cell Science · doi:10.1242/jcs.107.7.1725 · Cited by 169 · see citing works
A scalable method for integration and functional analysis of multiple microarray datasets
Huttenhower, C., Hibbs, M., Myers, C. L., & Troyanskaya, O. G. (2006) · Bioinformatics · doi:10.1093/bioinformatics/btl492 · Cited by 145 · see citing works
Self-citationEvolutionary plasticity of genetic interaction networks
Tischler, J., Lehner, B., & Fraser, A. G. (2008) · Nature Genetics · doi:10.1038/ng.114 · Cited by 129 · see citing works
The Sleipnir library for computational functional genomics
Huttenhower, C., Schroeder, M., Chikina, M. D., & Troyanskaya, O. G. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn237 · Cited by 81 · see citing works
Molecular genetic analysis of the calcineurin signaling pathways
Sugiura, R., Sio, S. O., Shuntoh, H., & Kuno*, T. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000855 · Cited by 68 · see citing works
Dynactin is involved in a checkpoint to monitor cell wall synthesis in Saccharomyces cerevisiae
Suzuki, M., Igarashi, R., Sekiya, M., Utsugi, T., Morishita, S., Yukawa, M., & Ohya, Y. (2004) · Nature Cell Biology · doi:10.1038/ncb1162 · Cited by 52 · see citing works
Kume, K., Koyano, T., Kanai, M., Toda, T., & Hirata, D. (2011) · Nature Cell Biology · doi:10.1038/ncb2166 · Cited by 41 · see citing works
Sunnerhagen, P., & Piškur, J. (2006) · Topics in current genetics · doi:10.1007/b95174 · Cited by 37 · see citing works
Schizosaccharomyces pombe comparative genomics; from sequence to systems
Wood, V. (2007) · Springer eBooks · doi:10.1007/4735_97 · Cited by 30 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Dixon SJ Fedyshyn Y Koh JLY Prasad TSK Chahwan C Chua G Toufighi K Baryshnikova A Hayles J Kim K-LHD-U Park H-O Myers CL Pandey A Durocher D Andrews BJ Boone C Significant conservation of synthetic lethal genetic interaction networks between distantly-related eukaryotes. Proc Natl Acad Sci USA 2008 105 16653 16658 10.1073/pnas.0806261105 18931302 PMC2575475 · DOI · Paper page
- Roguev A Bandyopadhyay S Zofall M Zhang K Fischer T Collins SR Qu H Shales M Park HO Hayles J Hoe KL Kim DU Ideker T Grewal SI Weissman JS Krogan NJ Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 2008 322 405 410 10.1126/science.1162609 18818364 PMC2753251 · DOI · Paper page
- Berglund AC Sjolund E Ostlund G Sonnhammer ELL InParanoid 6: eukaryotic ortholog clusters with inparalogs. Nucleic Acids Res 2008 36 D263 D266 18055500 PMC2238924
Cited by
Sorted by citations
A global genetic interaction network maps a wiring diagram of cellular function
Costanzo, M., VanderSluis, B., Koch, E. N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S. D., et al. (2016) · Science · doi:10.1126/science.aaf1420 · Cited by 1,240 · see citing works
Self-citationGenotype to phenotype: lessons from model organisms for human genetics
Lehner, B. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3404 · Cited by 228 · see citing works
Genetic Interaction Networks: Toward an Understanding of Heritability
Baryshnikova, A., Costanzo, M., Myers, C. L., Andrews, B., & Boone, C. M. (2013) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082509-141730 · Cited by 107 · see citing works
Self-citationGenetic interaction networks: better understand to better predict
Boucher, B., & Jenna, S. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00290 · Cited by 105 · see citing works
Quantitative genetic-interaction mapping in mammalian cells
Roguev, A., Talbot, D., Negri, G. L., Shales, M., Cagney, G., Bandyopadhyay, S., Panning, B., & Krogan, N. J. (2013) · Nature Methods · doi:10.1038/nmeth.2398 · Cited by 106 · see citing works
A yeast phenomic model for the gene interaction network modulating CFTR-ΔF508 protein biogenesis
Louie, R. J., Guo, J., Rodgers, J. W., White, R., Shah, N. A., Pagant, S., Kim, P., Livstone, M. S., Dolinski, K. J., McKinney, B. A., et al. (2012) · Genome Medicine · doi:10.1186/gm404 · Cited by 82 · see citing works
Environmental robustness of the global yeast genetic interaction network
Costanzo, M., Hou, J., Messier, V., Nelson, J., Rahman, M., VanderSluis, B., Wang, W., Pons, C., Ross, C., Ušaj, M., et al. (2021) · Science · doi:10.1126/science.abf8424 · Cited by 72 · see citing works
Self-citationConstraints and consequences of the emergence of amino acid repeats in eukaryotic proteins
Chavali, S., Chavali, P. L., Chalancon, G., de Groot, N. S., Gemayel, R., Latysheva, N. S., Ing‐Simmons, E., Verstrepen, K. J., Santhanam, B., & Babu, M. M. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3441 · Cited by 66 · see citing works
Saint, M., Bertaux, F., Tang, W., Sun, X.-M., Gamé, L., Köferle, A., Bähler, J., Shahrezaei, V., & Marguerat, S. (2019) · Nature Microbiology · doi:10.1038/s41564-018-0330-4 · Cited by 63 · see citing works
Systematic analysis of bypass suppression of essential genes
van Leeuwen, J. S., Pons, C., Tan, G., Wang, J. Z., Hou, J., Weile, J., Gebbia, M., Liang, W., Shuteriqi, E., Li, Z., et al. (2020) · Molecular Systems Biology · doi:10.15252/msb.20209828 · Cited by 52 · see citing works
Self-citationVanderSluis, B., Costanzo, M., Billmann, M., Ward, H. N., Myers, C. L., Andrews, B., & Boone, C. M. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2018.06.004 · Cited by 49 · see citing works
Self-citationEpigenetic epistatic interactions constrain the evolution of gene expression
Park, S., & Lehner, B. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.2 · Cited by 50 · see citing works
High-dimensional single-cell phenotyping reveals extensive haploinsufficiency
Ohnuki, S., & Ohya, Y. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2005130 · Cited by 43 · see citing works
Identifying Drivers of Parallel Evolution: A Regression Model Approach
Bailey, S. F., Guo, Q., & Bataillon, T. M. (2018) · Genome Biology and Evolution · doi:10.1093/gbe/evy210 · Cited by 42 · see citing works
Systematic analysis reveals the prevalence and principles of bypassable gene essentiality
Li, J., Wang, H.-T., Wang, W.-T., Zhang, X., Suo, F., Ren, J.-Y., Bi, Y., Xue, Y.-X., Hu, W., Dong, M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-08928-1 · Cited by 40 · see citing works
Prediction of Genetic Interactions Using Machine Learning and Network Properties
Madhukar, N. S., Elemento, O., & Pandey, G. (2015) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2015.00172 · Cited by 39 · see citing works
Searching for synergy in silico, in vitro and in vivo
Sucher, N. J. (2014) · Synergy · doi:10.1016/j.synres.2014.07.004 · Cited by 36 · see citing works
All or Nothing: Protein Complexes Flip Essentiality between Distantly Related Eukaryotes
Ryan, C. J., Krogan, N. J., Cunningham, P., & Cagney, G. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt074 · Cited by 35 · see citing works
Negative Functional Interaction Between Cell Integrity MAPK Pathway and Rho1 GTPase in Fission Yeast
Viana, R. A., Pinar, M., Soto, T., Coll, P. M., Cansado, J., & Pérez, P. (2013) · Genetics · doi:10.1534/genetics.113.154807 · Cited by 34 · see citing works
Synthetic Lethal Networks for Precision Oncology: Promises and Pitfalls
Shen, J. P., & Ideker, T. (2018) · Journal of Molecular Biology · doi:10.1016/j.jmb.2018.06.026 · Cited by 27 · see citing works
Global study of holistic morphological effectors in the budding yeast Saccharomyces cerevisiae
Suzuki, G., Wang, Y., Kubo, K., Hirata, E., Ohnuki, S., & Ohya, Y. (2018) · BMC Genomics · doi:10.1186/s12864-018-4526-z · Cited by 27 · see citing works
Cell-based screens and phenomics with fission yeast
Rallis, C., & Bähler, J. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1103205 · Cited by 23 · see citing works
Sun, H., Guo, Y., Lan, X., Jia, J., Cai, X., Zhang, G., Xie, J., Liang, Q., Li, Y., & Yu, G. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz930 · Cited by 20 · see citing works
Cańizares, D. G., del Río, S., Herrera, F., Ancede‐Gallardo, E., Antunes, A., & Agüero-Chapin, G. (2015) · BioMed Research International · doi:10.1155/2015/748681 · Cited by 18 · see citing works
Analysing the yeast complexome—the Complex Portal rising to the challenge
Meldal, B., Pons, C., Perfetto, L., del‐Toro, N., Wong, E. D., Aloy, P., Hermjakob, H., Orchard, S. E., & Porras, P. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab077 · Cited by 14 · see citing works
Characterization and Prediction of Haploinsufficiency Using Systems-Level Gene Properties in Yeast
Norris, M., Lovell, S. C., & Delneri, D. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.113.008144 · Cited by 13 · see citing works
Efficient strategies for screening large-scale genetic interaction networksPreprint
Deshpande, R., Nelson, J., Simpkins, S. W., Costanzo, M., Piotrowski, J. S., Li, S. C., Boone, C., & Myers, C. L. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/159632 · Cited by 11 · see citing works
Self-citationBig data mining powers fungal research: recent advances in fission yeast systems biology approaches
Wang, Z. (2016) · Current Genetics · doi:10.1007/s00294-016-0657-4 · Cited by 9 · see citing works
Data-driven identification of inherent features of eukaryotic stress-responsive genes
Latorre, P., Böttcher, R., Nadal‐Ribelles, M., Li, C. H., Solé, C., Martínez-Cebrián, G., Boutros, P. C., Posas, F., & de Nadal, E. (2022) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqac018 · Cited by 8 · see citing works
Billmann, M., Costanzo, M., Zhang, X., Hassan, A. Z., Rahman, M., Brown, K. R., Chan, K. S., Tong, A. H. Y., Pons, C., Ward, H. N., et al. (2026) · Cell · doi:10.1016/j.cell.2026.03.044 · Cited by 15 · see citing works
Self-citationÁcs-Szabó, L., Papp, L. A., Sipiczki, M., & Miklós, I. G. (2021) · Journal of Fungi · doi:10.3390/jof7100864 · Cited by 7 · see citing works
Computational Approaches to Identify Genetic Interactions for Cancer Therapeutics
Benstead-Hume, G., Wooller, S. K., & Pearl, F. M. G. (2017) · Journal of Integrative Bioinformatics · doi:10.1515/jib-2017-0027 · Cited by 9 · see citing works
Expanding interactome analyses beyond model eukaryotes
James, K., Wipat, A., & Cockell, S. (2022) · Briefings in Functional Genomics · doi:10.1093/bfgp/elac007 · Cited by 5 · see citing works
Effective Size and Effectiveness: Next Generation Sequencing and the Practice of Genomics in Africa
Ibrahim, M. E., & Musa, M. (2015) · Journal of Next Generation Sequencing & Applications · doi:10.4172/2469-9853.s1-008 · Cited by 5 · see citing works
A global genetic interaction map of a human cell reveals conserved principles of genetic networksPreprint
Billmann, M., Costanzo, M., Zhang, X., Hassan, A. Z., Rahman, M., Brown, K. R., Chan, K., Tong, A. H. Y., Pons, C., Ward, H. N., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.30.662193 · Cited by 5 · see citing works
Self-citationFan, J., Li, X. C., Crovella, M. E., & Leiserson, M. D. M. (2020) · Bioinformatics · doi:10.1093/bioinformatics/btaa818 · Cited by 3 · see citing works
Meta-analysis of dispensable essential genes and their interactions with bypass suppressors
Pons, C., & van Leeuwen, J. S. (2023) · Life Science Alliance · doi:10.26508/lsa.202302192 · Cited by 3 · see citing works
Identifying actionable synthetically lethal cancer gene pairs using mutual exclusivity
Wooller, S. K., Pearl, L. H., & Pearl, F. M. G. (2024) · FEBS Letters · doi:10.1002/1873-3468.14950 · Cited by 3 · see citing works
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · BMC Ecology and Evolution · doi:10.1186/s12862-021-01830-9 · Cited by 2 · see citing works
The distribution of fitness effects during adaptive walks using a simple genetic network
O’Brien, N. L. V., Holland, B. R., Engelstädter, J., & Ortíz-Barrientos, D. (2024) · PLoS Genetics · doi:10.1371/journal.pgen.1011289 · Cited by 2 · see citing works
The modifiers that cause changes in gene essentiality
Batté, A., Bosch-Guiteras, N., Pons, C., Ota, M., Lopes, M., Sharma, S., Tellini, N., Paltenghi, C., Conti, M. M., Kan, K. T., et al. (2026) · Cell Systems · doi:10.1016/j.cels.2025.101515 · Cited by 2 · see citing works
Dominance from the perspective of gene–gene and gene–chemical interactions
Gładki, A., Zielenkiewicz, P., & Kaczanowski, S. (2015) · Genetica · doi:10.1007/s10709-015-9875-9 · Cited by 2 · see citing works
Rough Sets in Ortholog Gene Detection
Cańizares, D. G., Sánchez, R. M., Lorenzo, M. M. G., Cardoso, G. C., Ábalo, R. G., & Arco, L. (2014) · Lecture notes in computer science · doi:10.1007/978-3-319-08729-0_15 · Cited by 1 · see citing works
Deineko, V., Kumar, A., Vlasblom, J., & Babu, M. (2015) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-23603-2_8 · Cited by 1 · see citing works
Big Data Supervised Pairwise Ortholog Detection in Yeasts
Cańizares, D. G., García, S. D. R., Herrera, F., Ancede‐Gallardo, E., Antunes, A., & Agüero-Chapin, G. (2017) · InTech eBooks · doi:10.5772/intechopen.70479 · Cited by 1 · see citing works
Qarles: a web server for the quick characterization of large sets of genes
Pons, C. (2025) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqaf030 · Cited by 1 · see citing works
Computational analysis of genome-scale growth-interaction data in Saccharomyces cerevisiae
VanderSluis, B. (2014) · University of Minnesota Digital Conservancy (University of Minnesota)
Mony, V. K. (2013) · K-State Research Exchange (Kansas State University)
Pairwise Ortholog Detection in Related Yeast Species by Using Big Data Supervised Classifications
Agüero-Chapin, G., Cańizares, D. G., García, S. D. R., Herrera, F., Ancede‐Gallardo, E., & Antunes, A. (2015) · MOL2NET International Conference on Multidisciplinary Sciences (MOL2NET) · doi:10.3390/mol2net-1-e002
Computational paradigms for analyzing genetic interaction networks
Pons, C., Costanzo, M., Boone, C. M., & Myers, C. L. (2015) · Cambridge University Press eBooks · doi:10.1017/cbo9781139012751.002
Self-citationComputational analysis of genetic interaction network structures and gene properties
Koch, E. N. (2017) · University of Minnesota Digital Conservancy (University of Minnesota)
Self-citationBarnes, M. R. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.735227371.793565853
Conservation of the genetic interaction network between two yeast speciesPreprint
Pons, C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.09.21.677604
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684584
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684575
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684581
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684587
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684560
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684578
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684566
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684599
Klim, J., Zielenkiewicz, U., Skoneczny, M., Skoneczna, A., Kurlandzka, A., & Kaczanowski, S. (2021) · Figshare · doi:10.6084/m9.figshare.14684572
Gene network centrality affects parallel evolution and local adaptation in wild yeastPreprint
Subramanian, S. K., & Bolnick, D. I. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.11.711091
- Authors
- Koch, E. N., Costanzo, M., Bellay, J., Deshpande, R., Chatfield-Reed, K., Chua, G., D'Urso, G., Andrews, B. J., Boone, C., & Myers, C. L.
- Affiliations
- University of Minnesota (US)
- University of Toronto (CA)
- University of Calgary (CA)
- Corresponding author
- Myers, Chad L
- Venue
- Genome Biology
- Published
- 2012-07-02
- Volume
- 13
- Issue
- 7
- Pages
- R57-R57
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC3491379
- OpenAlex
- W2111248446
- Cited by
- 68
- References
- 55
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 2 · 2023: 1 · 2022: 2 · 2021: 13 · 2020: 2 · 2019: 5 · 2018: 5 · 2017: 5 · 2016: 2 · 2015: 9 · 2014: 5 · 2013: 10 · 2012: 1
- FWCI
- 3.22
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Genome biology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- TSpace (University of Toronto) (submittedVersion)
- University Libraries (University of Maryland) (submittedVersion)
- Digital Repository at the University of Maryland (University of Maryland College Park)
- Funders
- National Science Foundation (0953881)
- National Institutes of Health
- Canadian Institutes of Health Research (MOP-57830)
- National Human Genome Research Institute (R01HG005084, R01HG005853)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Keywords
- synthetic genetic interactions, genetic interaction networks, network topology, Saccharomyces cerevisiae, Schizosaccharomyces pombe, cross-species prediction, orthologs, protein disorder, pleiotropy, gene expression variation, co-expression, evolutionary conservation
- MeSH terms
- Genes, Fungal, Models, Genetic, Mutation, Saccharomyces cerevisiae, Schizosaccharomyces, Species Specificity, Evolution, Molecular, Gene Regulatory Networks, Genetic Fitness
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
